Ecology, Evolution and Organismal Biology Ecology, Evolution and Organismal Biology Publications 2008 Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca Jeanne M. Serb Iowa State University, [email protected] Follow this and additional works at: http://lib.dr.iastate.edu/eeob_ag_pubs Part of the Ecology and Evolutionary Biology Commons, and the Marine Biology Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ eeob_ag_pubs/41. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Ecology, Evolution and Organismal Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Ecology, Evolution and Organismal Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca Abstract Several invertebrate systems have been developed to study various aspects of the eye and eye disease including Drosophila, Planaria, Platynereis, and most recently, the cubozoan jellyfish Tripedalia; however, molluscs, the second largest metazoan phylum, so far have been underrepresented in eye research. This is surprising as mollusc systems offer opportunities to study visual processes that may be altered by disease, vision physiology, development of the visual system, behavior, and evolution. Malacologists have labored for over a century as morphologists, systematists, physiologists, and ecologists in order to understand the structural and functional diversity in molluscs at all levels of biological organization. Yet, malacologists have had little opportunity to interact with researchers whose interests are restricted to the biology and development of eyes as model systems as they tend not to publish in the same journals or attend the same meetings. In an effort to highlight the advantages of molluscan eyes as a model system and encourage greater collaboration among researchers, I provide an overview of molluscan eye research from these two perspectives: eye researchers whose interests involve the development, physiology, and disease of the eye and malacologists who study the complete organism in its natural environment. I discuss the developmental and genetic information available for molluscan eyes and the need to place this work in an evolutionary perspective. Finally, I discuss how synergy between these two groups will advance eye research, broaden research in both fields, and aid in developing new molluscan models for eye research. Keywords retina, photoreceptor, opsin, Pax6 Disciplines Ecology and Evolutionary Biology | Marine Biology Comments This article is from American Malacological Bulletin 26 (2008): 3, doi:10.4003/006.026.0202. Posted with permission. This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/eeob_ag_pubs/41 Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca Author(s): Jeanne M. Serb Source: American Malacological Bulletin, 26(1/2):3-18. Published By: American Malacological Society DOI: http://dx.doi.org/10.4003/006.026.0202 URL: http://www.bioone.org/doi/full/10.4003/006.026.0202 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Amer. Malac. Bull. 26: 3-18 (2008) Toward developing models to study the disease, ecology, and evolution of the eye in Mollusca* Jeanne M. Serb Department of Ecology, Evolution and Organismal Biology, 253 Bessey Hall, Iowa State University, Ames, Iowa 50011, U.S.A., [email protected] Abstract: Several invertebrate systems have been developed to study various aspects of the eye and eye disease including Drosophila, Planaria, Platynereis, and most recently, the cubozoan jellyfish Tripedalia; however, molluscs, the second largest metazoan phylum, so far have been underrepresented in eye research. This is surprising as mollusc systems offer opportunities to study visual processes that may be altered by disease, vision physiology, development of the visual system, behavior, and evolution. Malacologists have labored for over a century as morphologists, systematists, physiologists, and ecologists in order to understand the structural and functional diversity in molluscs at all levels of biological organization. Yet, malacologists have had little opportunity to interact with researchers whose interests are restricted to the biology and development of eyes as model systems as they tend not to publish in the same journals or attend the same meetings. In an effort to highlight the advantages of molluscan eyes as a model system and encourage greater collaboration among researchers, I provide an overview of molluscan eye research from these two perspectives: eye researchers whose interests involve the development, physiology, and disease of the eye and malacologists who study the complete organism in its natural environment. I discuss the developmental and genetic information available for molluscan eyes and the need to place this work in an evolutionary perspective. Finally, I discuss how synergy between these two groups will advance eye research, broaden research in both fields, and aid in developing new molluscan models for eye research. Key words: retina, photoreceptor, opsin, Pax6 Traditional model systems to study eyes dition to exploring cellular biology, researchers have There is a great diversity of metazoans, but research on determined the molecular basis of eye specification by ge- developmental processes has largely focused on a small netically dissecting the fly eye to understand how it works. number of “representative” species. The traditional “big six” We have discovered how a group of multipotent cells (stem model organisms used in developmental biology are the cells) can be converted to eye primordia during eye organo- roundworm Caenorhabditis elegans, the fly Drosophila mel- genesis and have identified the set of nuclear genes that anogaster, the zebrafish Danio rerio, the African clawed frog regulate retinal specification. Understanding these genetic Xenopus laevis, the chicken Gallus gallus, and the mouse Mus mechanisms involved in eye formation gives researchers cru- musculus. These species were developed as model organisms cial information on the origin of eye disease—which is when because they are amenable to experimental and/or genetic the genetic program goes wrong. manipulation and possess life history characteristics suitable for life in the laboratory, i.e., they are easy to obtain, breed The Pax6 paradigm readily, and are fecund. Research focused on these six model Comparative work with the Drosophila eye and verte- animals has resulted in large-scale genome sequencing ef- brate eye indicates that all eyes may share a similar devel- forts, and complete or near complete inventories of genes opmental pathway in eye formation (Fig. 1). This has been and high-resolution genome maps are now available for all referred to as the eyeless/Pax6 paradigm (Donner and Maas six species (Waterson et al. 2002). 2004), which states that a single homologous genetic net- Of the two traditional invertebrate models, Caenorhab- work regulates eye formation, regardless of eye type, across ditis elegans and Drosophila melanogaster, only Drosophila all metazoans, and the Pax6 gene or its homologs are part of possesses eyes. The Drosophila compound eye has been an this regulatory gene network (Fig. 1A). There are three lines outstanding model system to study many general develop- of evidence for this conclusion. First, the gene eyeless (ey)in mental processes including cell fate specification, cell divi- Drosophila is homologous to the genes Small eye of mice and sion, growth, and death (Pappu and Mardon 2004). In ad- Aniridia of humans (Quiring et al. 1994). These two verte- * From the symposium “Molluscan models: Advancing our understanding of the eye” presented at the World Congress of Malacology, held from 15 to 20 July 2007 in Antwerp, Belgium. Co-sponsored by the National Science Foundation and the American Malacological Society. 3 4 AMERICAN MALACOLOGICAL BULLETIN 26 • 1/2 • 2008 general evolutionary processes. Further, studying the eyes in multiple species expands our understanding of variation among eye types, how similar visual tasks many be per- formed under different conditions, how permutations at the structural level affect performance, and how gene and gene pathways evolve to create new phenotypes and subsequently,